The evolution of information in the major transitions

Maynard Smith and Szathmáry's analysis of the major transitions in evolution was based on changes in the way information is stored, transmitted and interpreted. With the exception of the transition to human linguistic societies, their discussion centred on changes in DNA and the genetic system. We argue that information transmitted by non-genetic means has played a key role in the major transitions, and that new and modified ways of transmitting non-DNA information resulted from them. We compare and attempt to categorise the major transitions, and suggest that the transition from RNA as both gene and enzyme to DNA as genetic material and proteins as enzymes may have been a double one. Unlike Maynard Smith and Szathmáry, we regard the emergence of the nervous system as a major transition. The evolution of a nervous system not only changed the way that information was transmitted between cells and profoundly altered the nature of the individuals in which it was present, it also led to a new type of heredity-social and cultural heredity-based on the transmission of behaviourally acquired information.     

Temperature dependence of evolutionary diversification: differences between two contrasting model taxa support the metabolic theory of ecology

Biodiversity patterns are largely determined by variation of diversification rates across clades and geographic regions. Although there are multiple reasons for this variation, it has been hypothesized that metabolic rate is the crucial driver of diversification of evolutionary lineages. According to the metabolic theory of ecology (MTE), metabolic rate – and consequently speciation – is driven mainly by body size and environmental temperature. As environmental temperature affects metabolic rate in ecto‐ and endotherms differently, its impact on diversification rate should also differ between the two types of organisms. Employing two independent approaches, we analysed correlates of speciation rates and, ultimately, net diversification rates for two contrasting taxa: plethodontid salamanders and carnivoran mammals. Whereas in the ectothermic plethodontids speciation rates positively correlated with environmental temperature, in the endothermic carnivorans a reverse, negative correlation was detected. These findings comply with predictions of the MTE and suggest that similar geographic patterns of biodiversity across taxa (e.g. ecto‐ and endotherms) might have been generated by different ecological and evolutionary processes.     

Natural selection. III. Selection versus transmission and the levels of selection

George Williams defined an evolutionary unit as hereditary information for which the selection bias between competing units dominates the informational decay caused by imperfect transmission. In this article, I extend Williams' approach to show that the ratio of selection bias to transmission bias provides a unifying framework for diverse biological problems. Specific examples include Haldane and Lande's mutation-selection balance, Eigen's error threshold and quasispecies, Van Valen's clade selection, Price's multilevel formulation of group selection, Szathmáry and Demeter's evolutionary origin of primitive cells, Levin and Bull's short-sighted evolution of HIV virulence, Frank's timescale analysis of microbial metabolism and Maynard Smith and Szathmáry's major transitions in evolution. The insights from these diverse applications lead to a deeper understanding of kin selection, group selection, multilevel evolutionary analysis and the philosophical problems of evolutionary units and individuality.     

Emergence of protocellular growth laws

Template-directed replication is known to obey a parabolic growth law due to product inhibition (Sievers & Von Kiedrowski 1994 Nature 369, 221; Lee et al. 1996 Nature 382, 525; Varga & Szathmáry 1997 Bull. Math. Biol. 59, 1145). We investigate a template-directed replication with a coupled template catalysed lipid aggregate production as a model of a minimal protocell and show analytically that the autocatalytic template-container feedback ensures balanced exponential replication kinetics; both the genes and the container grow exponentially with the same exponent. The parabolic gene replication does not limit the protocellular growth, and a detailed stoichiometric control of the individual protocell components is not necessary to ensure a balanced gene-container growth as conjectured by various authors (Gánti 2004 Chemoton theory). Our analysis also suggests that the exponential growth of most modern biological systems emerges from the inherent spatial quality of the container replication process as we show analytically how the internal gene and metabolic kinetics determine the cell population's generation time and not the growth law (Burdett & Kirkwood 1983 J. Theor. Biol. 103, 11-20; Novak et al. 1998 Biophys. Chem. 72, 185-200; Tyson et al. 2003 Curr. Opin. Cell Biol. 15, 221-231). Previous extensive replication reaction kinetic studies have mainly focused on template replication and have not included a coupling to metabolic container dynamics (Stadler et al. 2000 Bull. Math. Biol. 62, 1061-1086; Stadler & Stadler 2003 Adv. Comp. Syst. 6, 47). The reported results extend these investigations. Finally, the coordinated exponential gene-container growth law stemming from catalysis is an encouraging circumstance for the many experimental groups currently engaged in assembling self-replicating minimal artificial cells (Szostak 2001 et al. Nature 409, 387-390; Pohorille & Deamer 2002 Trends Biotech. 20 123-128; Rasmussen et al. 2004 Science 303, 963-965; Szathma ry 2005 Nature 433, 469-470; Luisi et al. 2006 Naturwissenschaften 93, 1-13).     

Philosophical foundations for the hierarchy of life

We review Evolution and the Levels of Selection by Samir Okasha. This important book provides a cohesive philosophical framework for understanding levels-of-selections problems in biology. Concerning evolutionary transitions, Okasha proposes that three stages characterize the shift from a lower level of selection to a higher one. We discuss the application of Okasha’s three-stage concept to the evolutionary transition from unicellularity to multicellularity in the volvocine green algae. Okasha’s concepts are a provocative step towards a more general understanding of the major evolutionary transitions; however, the application of certain ideas to the volvocine model system is not straightforward.     

Variation in scorpion metabolic rate and rate-temperature relationships: implications for the fundamental equation of the metabolic theory of ecology

The fundamental equation of the metabolic theory of ecology (MTE) indicates that most of the variation in metabolic rate are a consequence of variation in organismal size and environmental temperature. Although evolution is thought to minimize energy costs of nutrient transport, its effects on metabolic rate via adaptation, acclimatization or acclimation are considered small, and restricted mostly to variation in the scaling constant, b(0). This contrasts strongly with many conclusions of evolutionary physiology and life-history theory, making closer examination of the fundamental equation an important task for evolutionary biologists. Here we do so using scorpions as model organisms. First, we investigate the implications for the fundamental equation of metabolic rate variation and its temperature dependence in the scorpion Uroplectes carinatus following laboratory acclimation. During 22 days of acclimation at 25 degrees C metabolic rates declined significantly (from 127.4 to 78.2 microW; P = 0.0001) whereas mean body mass remained constant (367.9-369.1 mg; P = 0.999). In field-fresh scorpions, metabolic rate-temperature (MRT) relationships varied substantially within and among individuals, and therefore had low repeatability values (tau = 0.02) and no significant among-individual variation (P = 0.181). However, acclimation resulted in a decline in within-individual variation of MRT slopes which subsequently revealed significant differences among individuals (P = 0.0031) and resulted in a fourfold increase in repeatability values (tau = 0.08). These results highlight the fact that MRT relationships can show substantial, directional variation within individuals over time. Using a randomization model we demonstrate that the reduction in metabolic rate with acclimation while body mass remains constant causes a decline both in the value of the mass-scaling exponent and the coefficient of determination. Furthermore, interspecific comparisons of activation energy, E, demonstrated significant variation in scorpions (0.09-1.14 eV), with a mean value of 0.77 eV, significantly higher than the 0.6-0.7 eV predicted by the fundamental equation. Our results add to a growing body of work questioning both the theoretical basis and empirical support for the MTE, and suggest that alternative models of metabolic rate variation incorporating explicit consideration of life history evolution deserve further scrutiny.     

Herbivore metabolism and stoichiometry each constrain herbivory at different organizational scales across ecosystems

Plant-herbivore interactions mediate the trophic structure of ecosystems. We use a comprehensive data set extracted from the literature to test the relative explanatory power of two contrasting bodies of ecological theory, the metabolic theory of ecology (MTE) and ecological stoichiometry (ES), for per-capita and population-level rates of herbivory across ecosystems. We found that ambient temperature and herbivore body size (MTE) as well as stoichiometric mismatch (ES) both constrained herbivory, but at different scales of biological organization. Herbivore body size, which varied over 11 orders of magnitude, was the primary factor explaining variation in per-capita rates of herbivory. Stoichiometric mismatch explained more variation in population-level herbivory rates and also in per-capita rates when we examined data from within functionally similar trophic groups (e.g. zooplankton). Thus, predictions from metabolic and stoichiometric theories offer complementary explanations for patterns of herbivory that operate at different scales of biological organization.     

The offspring-development-time/offspring-number trade-off

The metabolic theory of ecology (MTE) states that metabolic rate, ruled mainly by individual mass and temperature, determines many other biological rates. This view of ecology as ruled by the laws of physics and thermodynamics contrasts with life-history-optimization (LHO) theories, where traits are shaped by evolutionary processes. Integrating the MTE and LHO can lead, however, to a synthetic theory of ecology. In this work, we link the two theories to show that offspring development time is the result of both maternal investment in offspring and the metabolic constraints on offspring growth. We formulate a model that captures how offspring development time is the consequence of both offspring growth rate, determined by temperature and allometric scaling in accordance with the MTE, and the size reached by offspring at the end of the developmental period, determined mainly by LHO and reproductive strategies. We first extend the trade-off between offspring size and offspring number to ectotherms, showing that increased body temperatures result in increased resources available for reproduction. We then combine this trade-off with the general ontogenetic growth model to show that there is a trade-off between the number of offspring produced and offspring development time. The model predicts a shorter developmental time in organisms producing larger numbers of offspring.     

Neo-Darwinism,niche construction theory,and the initial domestication of plants and animals

The initial domestication of plants and animals and the subsequent emergence of agricultural economies, which began independently more than 10,000 years ago in a number of different world regions, represent a major evolutionary transition in earth history. It is these domesticates, and the agricultural economies based on them, that have formed the lever with which humans have substantially modified the earth’s terrestrial ecosystems over the past ten millennia. General explanations for this transition from hunting and gathering to food production economies formulated over the past 40 years have been based on standard evolutionary theory (SET) and employ the assumption of unidirectional adaptation—that environments change and species adapt. Here I compare these proposed SET—based externalist explanations for domestication with a recently formulated alternative developed from niche construction theory (NCT). Archaeological and paleoenvironmental records from two independent centers of domestication in the Americas—eastern North America and the Neotropics of northern South America, are found to support the NCT-based explanatory approach but not the SET explanations, underscoring the limitations of externalist SET approaches and the need for broader conceptualization of the processes that direct evolutionary change in order to gain a better general understanding of initial domestication as well as other major evolutionary transitions.     

The emerging structure of the Extended Evolutionary Synthesis: where does Evo-Devo fit in?

The Extended Evolutionary Synthesis (EES) debate is gaining ground in contemporary evolutionary biology. In parallel, a number of philosophical standpoints have emerged in an attempt to clarify what exactly is represented by the EES. For Massimo Pigliucci, we are in the wake of the newest instantiation of a persisting Kuhnian paradigm; in contrast, Telmo Pievani has contended that the transition to an EES could be best represented as a progressive reformation of a prior Lakatosian scientific research program, with the extension of its Neo-Darwinian core and the addition of a brand-new protective belt of assumptions and auxiliary hypotheses. Here, we argue that those philosophical vantage points are not the only ways to interpret what current proposals to ‘extend’ the Modern Synthesis-derived ‘standard evolutionary theory’ (SET) entail in terms of theoretical change in evolutionary biology. We specifically propose the image of the emergent EES as a vast network of models and interweaved representations that, instantiated in diverse practices, are connected and related in multiple ways. Under that assumption, the EES could be articulated around a paraconsistent network of evolutionary theories (including some elements of the SET), as well as models, practices and representation systems of contemporary evolutionary biology, with edges and nodes that change their position and centrality as a consequence of the co-construction and stabilization of facts and historical discussions revolving around the epistemic goals of this area of the life sciences. We then critically examine the purported structure of the EES—published by Laland and collaborators in 2015—in light of our own network-based proposal. Finally, we consider which epistemic units of Evo-Devo are present or still missing from the EES, in preparation for further analyses of the topic of explanatory integration in this conceptual framework.     

Metabolic theory or metabolic models?

The metabolic theory of ecology (MTE) claims to derive ecological relationships from the structure of resource distribution networks, which is assumed to determine the scaling of metabolism with body mass, and from the effect of temperature on the rate of biological processes. MTE is controversial. I propose that some of the controversy stems from the implicit adoption of different views of science by the proponents and critics of MTE. The perspective of proponents is consistent with the theory-centric view of science called the received view, whereas many of the critics implicitly adopt an alternative view consistent with a model-centric view of science. I propose that adopting the model-centric view can help to settle some of the differences among proponents and critics of MTE.     

Probabilistic causation and the explanatory role of natural selection

The explanatory role of natural selection is one of the long-term debates in evolutionary biology. Nevertheless, the consensus has been slippery because conceptual confusions and the absence of a unified, formal causal model that integrates different explanatory scopes of natural selection. In this study we attempt to examine two questions: (i) What can the theory of natural selection explain? and (ii) Is there a causal or explanatory model that integrates all natural selection explananda? For the first question, we argue that five explananda have been assigned to the theory of natural selection and that four of them may be actually considered explananda of natural selection. For the second question, we claim that a probabilistic conception of causality and the statistical relevance concept of explanation are both good models for understanding the explanatory role of natural selection. We review the biological and philosophical disputes about the explanatory role of natural selection and formalize some explananda in probabilistic terms using classical results from population genetics. Most of these explananda have been discussed in philosophical terms but some of them have been mixed up and confused. We analyze and set the limits of these problems.     

MEASURING EVOLUTIONARY CONSTRAINTS: A MARKOV MODEL FOR PHYLOGENETIC TRANSITIONS AMONG SEED DISPERSAL SYNDROMES

I introduce a Markov probabilistic model of transitions among discrete morphological states as a method for describing and testing nonrandom patterns of evolutionary change. The Markov model assumes one-generational dependency, i.e., that the future direction of evolutionary change depends on the current morphology of a species, not on any history of changes. This model is very flexible, allowing for any number of discrete states to describe morphology, yet permit rigorous testing of even complex evolutionary hypotheses. I apply this model to changes in seed dispersal mechanisms within 571 genera of Neotropical plants, using cladistic methods to infer the ancestral and derived states within each genus. I then test a series of progressively more complex hypotheses about the constraints that might shape the patterns of observed evolutionary transitions: 1) no transition constraints; 2) all dispersal mechanisms are equally labile evolutionarily; 3) the probability of particular evolutionary transitions among dispersal mechanisms depends on the descendant state but not on the ancestral state; 4) transition probabilities differ among pairs of dispersal mechanisms, but are reciprocal within such pairs. More complex hypotheses matched the data significantly better than did simpler hypotheses. However, only one of the hypotheses (reciprocal transitions) fit the observed data and then only for the most cautious interpretation of the frequencies of transitions within genera. These results suggest that evolutionary transitions among major adaptive syndromes are indeed ordered, and the observed patterns of transitions suggest possible reasons for such macroevolutionary structure.     

Major life-history transitions by deterministic directional natural selection

For large-scale evolution on Earth there has been a directional change where simple self-replicators evolved into large organisms with high metabolic rates and long pre-reproductive periods. Associated with this increase there have been major life-history transitions from asomatic, non-senescing, haploid, and asexually reproducing organisms to somatic, senescing, diploid, and sexually reproducing organisms with male and female individuals. Using a game theoretical model, it is shown that this trajectory can be explained by deterministic natural selection as it arises from first principles of the self-replication process in mobile organisms. It is shown (i) that selection for an increase in the energetic state of the organism puts a direction to evolution, (ii) that selection by density-dependent competitive interactions can explain the major life-history transitions as a function of the energetic state of the organism, and (iii) that the two selection processes combined can explain an exponentially increasing body mass. It is also shown (iv) why, for the case with an increasing body mass, we may expect many life histories to evolve in accordance with the exponents of the body mass allometries, (v) that an upper constraint on the body mass and metabolic rate can induce an additional transition into eusocial communities, and (vi) that the evolutionary trajectory is likely reversible with backward evolution during periods of environmental crises.     

The other eukaryotes in light of evolutionary protistology

In order to introduce protists to philosophers, we outline the diversity, classification, and evolutionary importance of these eukaryotic microorganisms. We argue that an evolutionary understanding of protists is crucial for understanding eukaryotes in general. More specifically, evolutionary protistology shows how the emphasis on understanding evolutionary phenomena through a phylogeny-based comparative approach constrains and underpins any more abstract account of why certain organismal features evolved in the early history of eukaryotes. We focus on three crucial episodes of this history: the origins of multicellularity, the origin of sex, and the origin of the eukaryote cell. Despite ongoing uncertainty about where the root of the eukaryote tree lies, and residual questions about the precise endosymbioses that have produced a diversity of photosynthesizing eukaryotes, evolutionary protistology has illuminated with considerable clarity many aspects of protist evolution. Our main message in light of evolutionary protistology is that these ‘other eukaryotes’ are in fact the organisms through which the rest of the eukaryotes should be understood.     

DIFFERENCES IN THE TIMING OF PRECHONDROGENIC LIMB DEVELOPMENT IN MAMMALS: THE MARSUPIAL–PLACENTAL DICHOTOMY RESOLVED

In contrast to placentals, marsupials are born with forelimbs that are greatly developmentally advanced relative to their hind limbs. Despite significant interest, we still do not know why this is the case, or how this difference is achieved developmentally. Studies of prechondrogenic and chondrogenic limbs have supported the traditional hypothesis that marsupial forelimb development is accelerated in response to the functional requirements of the newborn's crawl to the teat. However, limb ossification studies have concluded that, rather than the forelimb being accelerated, hind limb development is delayed. By increasing the taxonomic coverage and number of prechondrogenic events relative to previous studies, and combining traditional phylogenetic analyses of event sequences with novel analyses of relative developmental rates, this study demonstrates that the timing of limb development in marsupials is more complex than commonly thought. The marsupial phenotype was derived through two independent evolutionary changes in developmental rate: (1) an acceleration of the forelimb's first appearance and (2) a delay of hind limb development from the bud stage onward. Surprisingly, this study also provides some support for an evolutionary acceleration of the marsupial hind limb's first appearance. Further study is needed on the developmental and genetic mechanisms driving these major evolutionary transitions.     

Survival of replicators with parabolic growth tendency and exponential decay

The claim that the competition of parabolically growing self-replicators leads to dynamically stable coexistence was challenged by Lifson & Lifson [(1999). J. theor. Biol.199, 425-433]. They have shown that, if single- and double-strands are treated separately, and only single-strands undergo spontaneous decay, then there is natural selection rather than survival of everybody. We use their models to show that if double-strand decay is not neglected, then dynamical coexistence is still possible under a wide range of parameter values, in agreement with the chromatographized replicator model of von Kiedrowski & Szathmáry [(2000). Selection 1-3, 173-179]. Coexistence is always ensured above a critical resource (monomer) inflow rate. Recycling of decayed replicators into monomers further favours dynamical coexistence. The claim that parabolic growth invariably results in coexistence remains valid for the model for which it was meant to apply, namely for parabolic growth without template decay. Exponential decay acting on single- and double-strands, combined with parabolic growth, may or may not result in a dynamical coexistence of self-replicators.     

Selfishness versus functional cooperation in a stochastic protocell model

How to design an “evolvable” artificial system capable to increase in complexity? Although Darwin’s theory of evolution by natural selection obviously offers a firm foundation, little hope of success seems to be expected from the explanatory adequacy of modern evolutionary theory, which does a good job at explaining what has already happened but remains practically helpless at predicting what will occur. However, the study of the major transitions in evolution clearly suggests that increases in complexity have occurred on those occasions when the conflicting interests between competing individuals were partly subjugated. This immediately raises the issue about “levels of selection” in evolutionary biology, and the idea that multi-level selection scenarios are required for complexity to emerge. After analyzing the dynamical behaviour of competing replicators within compartments, we show here that a proliferation of differentiated catalysts and/or improvement of catalytic efficiency of ribozymes can potentially evolve in properly designed artificial cells where the strong internal competition between the different species of replicators is somewhat prevented (i.e., by choosing them with equal probability). Experimental evolution in these systems will likely stand as beautiful examples of artificial adaptive systems, and will provide new insights to understand possible evolutionary paths to the evolution of metabolic complexity.